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Layer VI in Cat Primary Auditory Cortex: Golgi Study and Sublaminar Origins of Projection Neurons

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Layer VI in Cat Primary Auditory Cortex: Golgi Study and Sublaminar Origins of Projection Neurons THE JOURNAL OF COMPARATIVE NEUROLOGY 404:332–358 (1999) Layer VI in Cat Primary Auditory Cortex: Golgi Study and Sublaminar Origins of Projection Neurons JORGE J. PRIETO1* AND JEFFERY A. WINER2 1Department of Histology, Institute of Neurosciences, University Miguel Herna´ ndez, 03550 San Juan, Alicante, Spain 2Division of Neurobiology, Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California 94720–3200 ABSTRACT The organization of layer VI in cat primary auditory cortex (AI) was studied in mature specimens. Golgi-impregnated neurons were classified on the basis of their dendritic and somatic form. Ipsilateral and contralateral projection neurons and the corticogeniculate cells of origin were labeled with retrograde tracers and their profiles were compared with the results from Golgi studies. Layer VI was divided into a superficial half (layer VIa) with many pyramidal neurons and a deeper part (layer VIb) that is dominated by horizontal cells. Nine types of neuron were identified; four classes had subvarieties. Classical pyramidal cells and star, fusiform, tangential, and inverted pyramidal cells occur. Nonpyramidal neurons were Martinotti, multipolar stellate, bipolar, and horizontal cells. This variety of neurons distin- guished layer VI from other AI layers. Pyramidal neuron dendrites contributed to the vertical, modular organization in AI, although their apical processes did not project beyond layer IV. Their axons had vertical, intrinsic processes as well as corticofugal branches. Horizontal cell dendrites extended laterally up to 700 µm and could integrate thalamic input across wide expanses of the tonotopic domain. Connectional experiments confirmed the sublaminar arrangement seen in Nissl material. Commissural cells were concentrated in layer VIa, whereas corticocortical neurons were more numerous in layer VIb. Corticothalamic cells were distributed more equally. The cytological complexity and diverse connections of layer VI may relate to a possible role in cortical development. Layer VI contained most of the neuronal types found in other layers in AI, and these cells form many of the same intrinsic and corticofugal connections that neurons in other layers will assume in adulthood. Layer VI, thus, may play a fundamental ontogenetic role in the construction and early function of the cortex. J. Comp. Neurol. 404:332–358, 1999. ௠ 1999 Wiley-Liss, Inc. Indexing terms: pyramidal cells; nonpyramidal cells; connections; cortical circuits; columnar organization Layer VI has a special role in sensory neocortex because al., 1985). The more restricted connectivity of layer IV is of its diverse connections. It is a source of corticofugal complemented by a neuronal architecture in which only a projections to the thalamus (Kelly and Wong, 1981), a few types of primarily nonpyramidal cells occur (Winer, target of thalamic input (Sousa-Pinto, 1973), a significant 1984a). Far more data are available on layer IV (Lund et origin for and terminus of the ipsilateral corticocortical al., 1981 [macaque monkey]) than on layer VI (To¨mbo¨l, pathways (Winguth and Winer, 1986), an important compo- nent in the commissural system (Code and Winer, 1985), and it participates in intrinsic interlaminar connections Grant sponsor: Direccio´n General de Investigacio´n en Ciencia y Tecno- (Usrey and Fitzpatrick, 1996 [tree shrew]). Such a wide log´ıa (DGICYT); Grant numbers: PB93–0928 and PM96–0082; Grant range of connections distinguishes it from layer IV, which sponsor: National Institutes of Health; Grant number: R01 DC02319–18. receives specific thalamocortical input (Davis and Ster- *Correspondence to: Jorge J. Prieto, M.D., Ph.D., Department of Histol- ogy, Institute of Neuroscience, University Miguel Herna´ ndez, Carretera ling, 1979) and the powerful projections from which are Valencia s/n, 03550 San Juan, Alicante, Spain. E-mail: [email protected] limited to the ipsilateral corticocortical system (Meyer and Received 13 April 1998; Revised 11 September 1998; Accepted 17 Albus, 1981) and to local interlaminar circuits (Mitani et September 1998 ௠ 1999 WILEY-LISS, INC. LAYER VI IN CAT PRIMARY AUDITORY CORTEX 333 1984), and this difference accentuates how little is known Histology about the role of layer VI in cortical function. The present study analyzes layer VI neurons in cat Tract-tracing experiments. Cortical injections were primary auditory cortex (AI). As the chief origin of the made into areas identified by their sulcal pattern and corticothalamic system, layer VI projections in other sys- corroborated later by architectonic analysis. Wheat germ tems may influence receptive field dynamics (Sillito et al., agglutinin conjugated to horseradish peroxidase (WGA- 1993), the augmenting response (Descheˆnes and Hu, 1990), HRP; 5%; Sigma Chemical Co., St. Louis, MO) in distilled the timing of relay cell discharge (Sillito et al., 1994), and water was injected by pressure through a glass micropi- the control of sensory gating (Crick, 1984), to name just a pette coupled to a Unimetrics syringe (Unimetric, Shore- few of the thalamic processes whose physiological basis wood, IL). Cortical tracer injections (six 0.2-µl deposits) might entail cortical control. The role of layer VI in into AI or the second auditory cortical area (AII; four 0.2-µl ipsilateral corticocortical projections and in the commis- injections) labeled commissural and ipsilateral corticocor- sural system is largely unknown. Our goal is to identify tical projection cells, respectively. Thalamic coordinates the resident neuronal populations and to relate these to were taken from standard atlases, and the volume of these specific projections. These data will enhance our perspec- deposits was 0.15 µl. The total number of experiments tive on the contribution of the infragranular layers to available was eight, including studies of corticocortical cortical and subcortical function. (n ϭ 3), commissural (n ϭ 3), and corticothalamic (n ϭ 2) projection systems. The technical procedures are pre- sented in detail in earlier studies of the commissural (Code MATERIALS AND METHODS and Winer, 1985, 1986) and ipsilateral corticocortical (Winguth and Winer, 1986) connections. The procedures used in this study have been described After a 3-day survival, the animals were reanesthetized previously in detail (Winer, 1984a–c, 1985, 1992). Proce- and perfused. Brains were sectioned on a freezing micro- dures were approved by and administered under the tome at 60 µm, and the sections were either developed for auspices of the appropriate institutional animal care and tetramethylbenzidine and counterstained with neutral red use committee. Adult cats of either sex and free of middle or incubated with diaminobenzidine and counterstained ear disease were used. Sodium pentobarbital (40 mg/kg, by using the Nissl method. i.p.) or isofluorane (1–4%, inhalant) were used to maintain Immunocytochemistry. The protocols for ␥-aminobu- stage III, plane ii of general anesthesia through perfusion tyric acid (GABA) and glutamate immunostaining have or surgery, respectively. been presented in detail in prior studies of cortical GABAer- gic neurons (Prieto et al., 1994a). Golgi material Neurons were impregnated with the Golgi-Cox method Data analysis (Cox, 1891) and by using the on-the-slide variation (Ramo´n- Only neurons that were encountered commonly in Golgi Moliner, 1970). Cells from more than 20 complete hemi- material were drawn and analyzed. Retrogradely labeled spheres, consisting of serial sections from the visual cortex neurons were classified by laminar location, somatic size through the somatic sensory cortex, were available. Neu- and shape, and dendritic arborization. The labeled neu- rons were classified by their laminar location, somatic rons were plotted and counted. A sample of 20 sections/ form, and dendritic arborization (Table 1). Axons rarely experiment through the region of maximum labeling was were impregnated. used. Abbreviations AAF anterior auditory field LM large multipolar cell aes anterior ectosylvian sulcus LP lateral posterior nucleus or large pyramidal cell AI primary auditory cortex M medial division of the medial geniculate body AII second auditory cortical area Ma Martinotti cell Bp bipolar cell MGBm medial geniculate body, medial division BV blood vessel MGBv medial geniculate body, ventral division CG central gray MM medium-sized multipolar cell CP cerebral peduncle MP medium-sized pyramidal cell D dorsal nucleus of the medial geniculate body OT optic tract DD deep dorsal nucleus of the medial geniculate body P posterior auditory field DS dorsal superficial nucleus of the medial geniculate body PC posterior commissure EPD posterior ectosylvian gyrus, dorsal part RN red nucleus EPI posterior ectosylvian gyrus, intermediate part SF/daz suprasylvian fringe/dorsal auditory zone EPP posterior ectosylvian gyrus, posterior part Sg suprageniculate nucleus EPV posterior ectosylvian gyrus, ventral part SM small multipolar cell FHP fusiform horizontal pyramidal cell SmP small pyramidal cell FVP fusiform vertical pyramidal cell StP star pyramidal cell GABA ␥-aminobutyric acid Te temporal cortex Glu glutamate TP tangential pyramidal cell H horizontal cell V ventral auditory field or ventral division of the medial Hyp hypothalamus geniculate body I–VIa,b cortical layers Vb ventrobasal nucleus of the thalamus Ins insular cortex VP ventral posterior auditory field IP inverted pyramidal cell wm white matter LGN lateral geniculate body 334 J.J. PRIETO AND J.A. WINER TABLE 1. Summary of Layer VI Cell Types in Cat Primary Auditory Cortex Number of Somatic shape primary Dendritic Dendritic Cell type Subtypes Sublayer(s)1 and size2 dendrites field shape field size2 Figure(s) 1. Pyramidal a. Small VIa, VIb Triangular; 14 ϫ 18 µm 4–5 Vertically elongated 280 ϫ 730 µm 4:1a; 15A–C:1a b. Medium-sized VIa, VIb Triangular; 18 ϫ 28 µm 5–9 Cylindrical 310 ϫ 800 µm 4:1b; 5; 7:1b; 15A–C:1b c. Large VIa Triangular; 36 ϫ 40 µm 7–9 Cylindrical 680 ϫ 1,100 µm 4:1c; 15A–C:1c 2. Star pyramidal — VIa, VIb Round; 20 ϫ 18 µm 6–8 Vertically elongated 240 ϫ 510 µm 6:2; 15A:2 3. Fusiform pyramidal a. Vertical VIa, VIb Fusiform; 10 ϫ 25 µm 2–4 Fusiform 180 ϫ 700 µm 6:3a; 15A–C:3a b.
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